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| REVIEW ARTICLE |
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| Year : 2018 | Volume
: 55
| Issue : 4 | Page : 318-326 |
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Barriers affecting uptake of cervical cancer screening in low and middle income countries: A systematic review
Pradeep Devarapalli, Satyanarayana Labani, Narayanasetti Nagarjuna, Poonam Panchal, Smita Asthana
Department of Epidemiology and Biostatistics, National Institute of Cancer Prevention and Research, Indian Council of Medical Research, I-7, Sector-39, Noida, Uttar Pradesh, India
| Date of Web Publication | 28-Feb-2019 |
Correspondence Address:
Smita Asthana
Department of Epidemiology and Biostatistics, National Institute of Cancer Prevention and Research, Indian Council of Medical Research, I-7, Sector-39, Noida, Uttar Pradesh
India
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/ijc.IJC_253_18
BACKGROUND: Cervical cancer is the second-most common cancer among women in the developing world and approximately 500,000 cases are diagnosed each year. In developed countries, cervical cancer (CCa) accounts for only 3.6% of newly diagnosed cancers. OBJECTIVE: The present study aims to identify the most effective barriers associated with CCa screening uptake in low and middle-income countries (L and MICs) and aid to adopt effective measures to overcome prevailing barriers to the attainment of CCa uptake in the community. MATERIALS AND METHODS: Health sciences electronic databases like MEDLINE, PubMed, Cochrane library, and Google Scholar were searched for studies published until August 2017. Keywords used for the search were (“cervical cancer screening”), (“barriers”), AND (“low income countries” OR “Middle income countries”). Articles were reviewed and data were extracted by using Mendeley Desktop Software (V-1.17.10). Income-level classification of countries was done as per the World Bank 2017 report. Statistical software like SPSS-V.23 and Medical-V.14 were used for the statistical application. RESULTS: A total of 31 studies met the inclusion criteria with a total of 25,650 participants. The sample size of the included studies ranged from 97 to 5929 participants. Articles majorly reported data on participants from African region (51.6%) and minimally in the Western Pacific region (3.2%). Sampling methods among studies varied from convenience sampling-12 (39.7%) to consecutive sampling-1 (3.2%). Besides, two studies (6.5%) did not discuss their sampling procedures. It was observed that “Lack of information about CCa and its treatment” (Barrier of lack of knowledge and Awareness); “Embracement or shy” (Psychological Barrier); “Lack of time” (structural Barrier); and “Lack of family support” (Sociocultural and religious barrier) were the most commonly reported among all 22 barriers. CONCLUSION: There is a need of policies advancement of CCa screening programs by focusing on aspects of accessibility, affordability, CCa education, and the necessity of screening to improve screening uptake to control the CCa morbidity and mortality rate in L and MIC's.
Keywords: Barriers, Cervical cancer, diagnosis, low income countries, middle income countries, screening uptake
How to cite this article:
Devarapalli P, Labani S, Nagarjuna N, Panchal P, Asthana S. Barriers affecting uptake of cervical cancer screening in low and middle income countries: A systematic review. Indian J Cancer 2018;55:318-26 |
How to cite this URL:
Devarapalli P, Labani S, Nagarjuna N, Panchal P, Asthana S. Barriers affecting uptake of cervical cancer screening in low and middle income countries: A systematic review. Indian J Cancer [serial online] 2018 [cited 2022 Jul 4];55:318-26. Available from: https://www.indianjcancer.com/text.asp?2018/55/4/318/253287 |
| » Introduction | |  |
Cervical cancer (CCa) is a preventable and curable malignant disease with a global annual crude incidence rate of 15.1 per 1,00,000.[1] An estimated 5, 29, 000 new cases and 2,75,000 deaths occurred in 2008 out of which 79–83% of new cases were diagnosed in developing countries.[2] For developed countries, CCa accounts for only 3.6% of newly diagnosed cancers [3] whereas it is the third most common cancer and fourth most common cause of cancer death in the world.[4]
CCa is the most preventable cancer due to its slow progression, cytologically identifiable precancerous lesions, and effective treatments.[5],[6] Evidence suggests that cervical screening awareness and early detection through screening had a major impact on mortality associated with CCa in developed nations like United States, United Kingdom, and Australia.[7],[8],[9] In developing countries, cervical screening programs failed to decrease the incidence and mortality of the disease due to the low uptake rate of screening.[10],[11],[12] The Papanicolaou (Pap) test, visual inspection with acetic acid (VIA), and Lugol's iodine (VILI) are effective screening methods for the early detection of CCa. The Pap-test can be performed in hospitals and clinics, whereas VIA does not require laboratory procedures and can be done in areas with less resources also. It has been observed that there are several barriers and factors which affect the uptake rate of cervical screening, i.e., accessibility to testing facilities, lack of health education, low socioeconomic status, low perceived risk of disease, fear of CCa diagnosis, fear of pain and embarrassment, lack of female health care providers, busy schedules, and beliefs that such tests are unnecessary.
Cervical screening programs in developing countries were not of priority earlier. To identify factors and barriers associated with cervical screening uptake prior to organizing community-based screening programs is essential. In low resource countries, identifying barriers and factors associated with low cervical screening uptake helps policy makers and health care delivery organizations to improve and take necessary steps to overcome the existing barriers and reach the community to increase the cervical screening uptake, which in turn may decrease the incidence and mortality of the disease. Primary studies have been conducted to identify the factors and barriers for uptake of cervical screening from various countries. Systematic reviews were also conducted on various aspects to increase screening uptake such as through the special event of health promotion.[13] Self-collection of Human papillomavirus (HPV) testing [14],[15] and other interventions.[16],[17] There was a systematic review done on barriers for CCa screening participation in developed countries like UK, Australia, Sweden, and Korea.[18] There have been integrated reviews of barriers to CCa screening from sub-Saharan Africa and Asia.[19],[20],[21] These systematic reviews were not focused toward low and middle-income countries. Since the factors and barriers from low and middle-income countries are likely to be very different from developed countries, hence, we conducted a systematic review of studies from low and middle income countries.
| » Materials and Methods | | |
Search strategy
We conducted a comprehensive search of quantitative literature that was published till August 2017 in the electronic databases MEDLINE, PubMed, Cochrane library, and Google Scholar to retrieve all English language studies that contained information on barriers of CCa screening in low and middle-income countries. Studies were defined into “low income,” “lower middle income,” and “upper middle income” countries as classified by the World Bank (World Bank, July 2016). Articles were included if they reported quantitative data of women's knowledge or experiences or observations or perceptions of cervical cancer screening in lower and middle income countries. Primary concepts of “cervical cancer screening” “barriers,” “low income and middle income countries” were expanded to generate additional medical terms (cervix, cervical, cancer, neoplasm, cervical neoplasms, screening, and primary diagnosis of cancer) for the search. The subject search and text word search were done separately in all databases and then combined with “OR” and “AND” operators. Combined terms were used, for example, (“cervical cancer screening” or 'cervical screening') AND ('barriers' or 'barriers in screening') AND (“low income countries” OR “middle income countries”). Gray literature and additional articles were identified using the bibliography of included articles and some excluded review articles, along with forward citation searches.
Study selection
Only articles that had reported quantitative evidence data of barriers on women's perception or experiences of cervical screening in low and middle-income countries were included. [Figure 1] shows the selection process of the articles retrieved. Our systematic review was done according to PRISMA guidelines (http://annals.org/article.aspx?articleid=744664). The initial database search retrieved 935 published English-language studies. The abstracts were read and studies that did not meet the inclusion criteria, of which 115 were duplicates and 720 studies were excluded because they were conducted either among woman with CCa receiving treatments or were conducted in high-income countries. Of the remaining 205 studies, 43 met the inclusion criteria of which 23 studies focused on barriers to CCa screening.[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39],[40],[41],[42],[43],[44],[45],[46],[47],[48],[49],[50],[51],[52] Included studies were published between 2002 and 2017. Further search was conducted using Google Scholar and additional articles were identified using the reference lists of included articles and excluded review articles, and forward citation searches.
Inclusion criteria
Population-based studies (cross-sectional studies, quasi-experimental, mixed and case–control studies) conducted in diverse settings like hospitals or communites published till August 2017. English language, low and middle-income countries (according to World Bank list of economies-July 2016) based studies of barriers and factors influencing cervical cancer and its screening uptake procedures. Studies with quantitative assessments were included.
Exclusion criteria
Case reports, case series, earlier reviews, and qualitative studies of CCa and its screening uptake. Studies conducted in high-income countries and articles published in languages other than English were excluded.
Data extraction and synthesis
We extracted the following key characteristics of the studies: lead author and country, year published, study design, sampling technique, sample size, age group and mean age, percentage rate of women ever screened and never screened, screening method used, and barriers themes with percentages. Articles were reviewed and data was extracted by using Mendeley Desktop Software (V-1.17.10). After the removal of duplicates, primary outcome data of all articles were indexed in Microsoft Excel. Later, interpretation of textual data was extracted to a Microsoft Word document. Income-level classification of countries was done as per the World Bank 2017 report (https://siteresources.worldbank.org/DATASTATISTICS/Resources/CLASS.XLS). Quantitative data of barriers were mainly categorized into 1. Barriers of lack of knowledge and awareness, 2. psychological barriers, 3. structural barriers, and 4. socio-cultural and religious barriers. Two authors (PD and NN) independently carried out the literature search and identified 935 citations for CCa screening by two investigators (PD and NN) independently. Full-text articles were identified and assessed for eligibility after applying the inclusion and exclusion criteria. Critical appraisal of each study found eligible was done by both investigators. Agreement of the requisite contents of the articles related to quality assessment and data extraction was performed. Any dispute in selection was resolved by author (SA) after deliberation with PD and NN. Statistical software like SPSS-V.23 and Medcal-V.14 was used for statistical application.
| » Results | | |
As per the selection criteria, approximately 28 of the 31 articles were published before 2010 and only 3 articles were published between 2002 and 2010. They included a total of 25,650 participants across the 31 independent studies. Included studies had different sampling methods in which most of them were population-based articles reported on recruitment in diverse settings i.e., hospitals or community and most of the respondents were patients or participants. Outcome measures for most of the studies included respondent's willingness to participate or perceived barriers to participation in CCa screening. The majority of the articles reported data on African participants (51.6%); fewer studies focused on Southeast Asians (16%), Americans (16%), Europeans (12.9%), and Western Pacific (3.2). cross-sectional studies (80.6%) following with quasi-experimental (12.9%), mixed,[27] and case–control [39] [Table 1]. | Table 1: Characteristics of studies of low and middle-income countries for CCa screening uptake and their effecting barriers
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The 31 studies were from Nigeria-7, Kenya-5, Turkey-4, India-3, Ethiopia-2, Mexico-3, Tanzania-2, Bangladesh-1, China-1, El Salvador-1, Jamaica-1, and Thailand-1. Among sampling methods 12 (38.7%) studies used convenience sampling, while 7 (22.6%) studies used random sampling followed by multistage sampling-6 (19.4%), systematic sampling-3 (9.7%), and consecutive sampling-1 (3.2%). Sampling procedures were not clearly discussed in two studies (6.5%).
The sample size of the quantitative studies ranged from 97 to 5929 participants.[38],[40] The age of the study participants in studies varied from 14 years and above, but 8 studies did not report any upper age limit. In 31 studies, most of them used interviewer-administered questionnaire (35.5%) followed by structured interviews (32.3%), questionnaire survey methodology (29%), and survey forms (3.2%).
Percentage of barriers reported in studies of low and middle-income countries is shown in [Table 2] and meta-analysis of proportions of reported barriers and their heterogeneity outcomes are shown in [Table 3]. | Table 2: Percentage of barriers reported in studies of low and middle income countries
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 | Table 3: Meta-analysis of proportions of reported barriers and their heterogeneity outcomes
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Barriers reported
Barriers of lack of knowledge and awareness
Among the 31 studies, 27 reported the association between barriers of lack of knowledge and awareness and reduced participation in trials (87.09). In addition, one of those studies reported lack of knowledge about the backgrounds of cancer and its treatment as a barrier to enrolment, followed by the 18 (58.06%) studies that reported barriers to awareness. The belief that only symptomatic women need to undergo CCa screening was the next frequently reported barrier (48.38%). Belief of virginity loss (6.45) was the least reported barrier among them [Figure 2].
Psychological barriers
A total of 28 articles have reported that psychological barriers were one of the reasons that effect in CCa screening uptake. Most of those articles reported embarrassment or shyness (45.16%) as a barrier during CCa screening procedures. Other frequently reported barriers in participating in CCa screening were painful procedures (41.93%), fear of getting diagnosed with CCa (35.48%), and anxiety or fear (38.7%) in CCa screening procedure [Figure 3].
Structural barriers
Lack of time for procedure and/or belief that the procedure (48.3%) was time consuming was the most frequently reported barrier in the eligible studies. Expensive CCa screening procedure was the next most reported barrier (41.93%). Lack of transportation to the CCa screening procedure center and insufficient medical advice from health care providers were the least reported barrier among structural barriers. Moreover, 25.8% of studies have reported that CCa screening centers were far to reach from their residences [Figure 4].
Sociocultural and religious barriers
Only 14 articles reported about sociocultural and religious barriers, in which lack of family support (husband's disapproval or condemnation of patients planning to undergo CCa screening procedure) was the most frequently reported barrier. About 6.45% of women believe that CCa screening is an unnecessary thing for an unmarried women [Figure 5].
Distribution of barriers among low and middle income countries
Low-income countries
The four studies that reported barriers for CCa screening in low-income countries were all from the African region namely Ethiopia (6.5%), Tanzania (6.5%). Lack of knowledge and awareness was the most commonly reported barrier than other barriers in LICs. In Ethiopia most (67%) felt that only symptomatic women should undergo screening.[42] In a study by Melissa et al., 90% Tanzanian women had never got screened for CCa. Two studies conducted in Ethiopia shows that percentages of women never had got screened for CCa screening were [42] - 80.1% and Fasika et al (89%) [Table 1].
Low-middle income countries (LMICs)
A total of 17 studies in low-middle income countries explored barriers for CCa screening, in which 7 studies were from Nigeria. Besides, 13 studies reported lack of information about CCa and its screening procedures as a common barrier to screening uptake. A study was undertaken in Nigeria also identified religious barrier- trust in God (8.8%). Lack of time, time taking procedure, distance to the screening center and expenses were some of the barriers that are majorly reported in these countries.[53],[54] A study conducted in India shows that 100% (n = 299) participants in the study had never got screened for CCa.
Upper-middle income countries (UMICs)
A total of 11 studies in upper-middle income countries were from Turkey-4, Mexico-3, China-1, Thailand-1, and Jamica-1 that had reported barriers for CCa screening. Structural barriers including cost associated with screening and treatment, distance to the service centres, access, and availability to screening were the most common barriers identified in these countries. This was followed by lack of awareness of, and knowledge about, CCa and CCa screening in eight studies and social and religious factors including marital status and lack of family support in another three studies.[37],[39],[40]
| » Discussion | | |
Our systematic review assessed the numerous barriers that affect the participation of women in low and middle income countries in CCa screening. Included studies of different countries framed barriers in different ways relying on factors like perceptions, cultures, education, and accessibility of screening services. However, poor understanding of the role of CCa and lack of knowledge about screening procedures were the major reported barriers among women in most studies from low and middle-income countries.
Most of the studies have reported that lack of knowledge is an important barrier perceived for CCa screening. The next majorly reported barriers are “Absence of any CCa symptoms” and “Lack of time for Screening” in which, eight studies of LMICs have reported “Absence of any CCa symptoms” as a barrier, followed by UMICs-5 and LICs-2. Whereas seven studies of LMICs have reported “Lack of time for screening”, followed by UMICs-6 and LICs-2. Long delays in the screening process may possibly effect in follow-up of treatment or for future screenings. It was known that most of the screening methods test the presence of precancerous cells in cervix. Low cost screening has a greater impact when it is targeted to women of ages between 30 and 40 in a low resource setting.[22] Besides, promoting self sampling in low resourced areas of developed countries had helped in improving access to cervical screening. It was also proved as a better way to attract non-attendees and recall their invitation for cytology and screening programs.[23] About 9.7% women reported poor facilitates, false negative results and untrained clinical professionals as the barriers. In earlier studies, it was estimated that 29.3% of failures to prevent invasive cervical cancer can be attributed to false-negative Pap smear More Detailss and 11.9% to poor follow-up of abnormal results.[24]
In many studies [33],[34],[35],[38],[41],[42],[43],[44],[49],[55],[56],[57],[58],[59] embarrassment or shyness was reported as a barrier due to the unfriendly or male work staff. Women in some studies also reported facing objection from their husbands or family members to take the screening test. In an earlier review, Asian immigrants held a variety of misconceptions concerning one's susceptibility to cancer and social stigmatization by community and physicians, whereas African–Americans identified administrative processes in establishing health care as barriers to screening.[25] Some studies have reported that women are discouraged by the cost of services or traveling far for procedure. Analyses of a previous review showed that liquid based cytology was more cost-effective than conventional Pap smear testing over the same screening interval.[26]
A study revealed that cervical cancer screening ranges from 1% in Bangladesh to 73% in Brazil. Particularly, poor and older women are less likely to be screened in developed(63%) and developing countries(19%) and have highest risk of getting cervical cancer.[27] There are several issues requiring further evaluation like appropriate screening interval, age to start and stop screening, the role of self-sampling for HPV testing and the choice of primary test (cytology and/or HPV).[28]
Limitations of the studies that might have influenced the results are lack of studies of particular defined data and studies from different geographical area and heterogeneity of diversified population data collected and pooled from various studies. Variations such as age range, sampling techniques, study designs, data collected methods were also not uniform. Merging such data may lead to high heterogeneity which is a potential source of bias. Nonadjustment of potential confounders in some primary studies can also be an issue.
Settings at the screening center also influence the screening uptake rate, such as infrastructure, cleanliness, lack of trained staff, malfunctioned equipment, etc. The lack of similarity between reported barriers of studies may be due to diversity in modes of recruitment, sample size, study designs, sampling procedures, and study quality. Even-though included studies have bias between them it is may be because of the unclear sampling procedures and different study domains. CCa screening is given less priority in low and middle income countries, resulting to either improper screening programs or being totally unavailable. Barriers do influence recruitment outcomes through their effects on opportunity to participate and the choice to refuse or accept participation. Greater levels of guiding knowledge is needed for development of CCa screening uptake. Advance research into the tools by which screening uptake will be increased is needed for future, so that they help to update policies in L and MICs.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| » References | | |
| 1. | Bruni L, Barrionuevo-Rosas L, Albero G, Aldea M, Serrano B, Valencia S, et al. ICO informationcentreon HPVandcancer (HPVinforma- tioncentre). Human papillomavirus and related diseases in the world. Summary Report 2015-04-08. Available from: http://www.hpvcentre.net/statistics/reports/XWX.pdf. [Last accessed on 2015 Nov 09].  |
| 2. | Varughese J, Richman S. Cancer care inequity for women in resource-poor countries. Rev Obstet Gynecol 2010;3:122-32. |
| 3. | Shafi MI, Earl HM, Tan LT. Gynecological Oncology. New York, NY, USA: Cambridge University Press; 2010. p. 2. |
| 4. | Institute for Health Metrics and Evaluation, The Challenge Ahead: Progress in Breast and Cervical Cancer, Institute for HealthMetrics and Evaluation, Seattle, Wash, USA, 2011. |
| 5. | Lee J, Seow A, Ling SL. Improving adherence to regular Pap smear screening among Asian women: A population- based study in Singapore. Health Educ Behav 2002;29:207-18. |
| 6. | Castellsagué X. Natural history and epidemiology of HPV infection and cervical cancer. Gynecol Oncol 2008; 110:S4-7. |
| 7. | Scarinci IC, Garcia FA, Kobetz E, Partridge EE, Brandt HM, Bell MC, et al. Cervical cancer prevention. Cancer 2010;116:2531-42. |
| 8. | Peto J, Gilham C, Fletcher O, Matthews FE. The cervical cancer epidemic that screening has prevented in the UK. Lancet 2004;364:249-56. |
| 9. | Taylor R, Morrell S, Mamoon H, Wain G, Ross J. Decline in cervical cancer incidence and mortality in New South Wales in relation to control activities - Australia. Cancer Causes Control 2006;17:299-306. |
| 10. | Jeong S, Saroha E, Knight J, Roofe M, Jolly PE. Determinants of adequate follow-up of an abnormal Papanicolaou result among Jamaican women in Portland, Jamaica. Cancer Epidemiol 2011;35:211-6. |
| 11. | Hoque M, Hoque E, Kader SB. Evaluation of cervical cancer screening program at a rural community of South Africa. East Afr J Public Health 2008;5:111-6. |
| 12. | |
| 13. | Escoffery C, Rodgers KC, Kegler MC, Haardorfer R, Howard DH, Liang S, et al. A systematic review of special events to promote breast, cervical and colorectal cancer screening in the United States. BMC Public Health 2014;14:274. |
| 14. | Racey CS, Withrow DR, Gesink D. Self-collected HPV testing improves participation in cervical cancer screening: A systematic review and meta-analysis. Can J Public Health 2013; 104:159-66. |
| 15. | Madzima TR, Vahabi M, Lofters A. Emerging role of HPV self-sampling in cervical cancer screening for hard-to-reach women: Focused literature review. Can Fam Physician 2017; 63:597-601. |
| 16. | Albrow R, Blomberg K, Kitchener H, Brabin L, Patnick J, Tishelman C, et al. Interventions to improve cervical cancer screening uptake amongst young women: A systematic review. Acta Oncol 2014;53:445-51. |
| 17. | Sabatino SA, Lawrence B, Elder R, Mercer SL, Wilson KM, DeVinney B, et al. Effectiveness of interventions to increase screening for breast, cervical, colorectal cancers: Nine updated systematic reviews for the guide to community preventive services. Am J Prev Med 2012;43:97-118. |
| 18. | Crawford J, Ahmad F, Beaton D, Bierman AS. Cancer screening behaviorsamong South Asian immigrants in the UK, US and Canada: A scoping study. Health Soc Care Community 2016;24:123-53. |
| 19. | McFarland DM, Gueldner SM, Mogobe KD. Integrated review of barriers to cervical cancer screening in Sub-Saharan Africa. J Nurs Scholarsh 2016;48;490-8. |
| 20. | Lim JN, Ojo AA. Barriers to utilization of cervical cancer screening in Sub Sahara Africa: A systematic review. Eur J Cancer Care (Engl) 2017;26. doi: 10.1111/ecc. 12444. |
| 21. | Lu M, Moritz S, Lorenzetti D, Sykes L, Straus S, Quan H. A systematic review of interventions to increase breast and cervical cancer screening uptake among Asian women. BMC Public Health 2012;12:413. |
| 22. | WHO. Comprehensive Cervical Cancer Control: A Guide to Essential Practice. 2 nd ed. Geneva: World Health Organization; 2014. |
| 23. | Snijders PJ, Verhoef VM, Arbyn M, Ogilvie G, Minozzi S, Banzi R, et al. High-risk HPV testing on self-sampled versus clinician-collected specimens: A review on the clinical accuracy and impact on population attendance in cervical cancer screening. Int J Cancer 2013;132:2223-36. |
| 24. | Spence AR, Goggin P, Franco EL. Process of care failures in invasive cervical cancer: Systematic review and meta-analysis. Prev Med 2007;45:93-106. |
| 25. | Johnson CE, Mues KE, Mayne SL, Kiblawi AN. Cervical cancer screening among immigrants and ethnic minorities: A systematic review using the Health Belief Model. J Low Genit Tract Dis 2008;12:232-41. |
| 26. | Karnon J, Peters J, Platt J, Chilcott J, McGoogan E, Brewer N. Liquid-based cytology in cervical screening: An updated rapid and systematic review and economic analysis. Health Technol Assess 2004;8:iii, 1-78. |
| 27. | Gakidou E, Nordhagen S, Obermeyer Z. Coverage of cervical cancer screening in 57 countries: Low average levels and large inequalities. PLoS Med 2008;5:e132. |
| 28. | Cuzick J, Sasieni P, Davies P, Adams J, Normand C, Frater A, et al. A systematic review of the role of human papilloma virus (HPV) testing within a cervical screening programme: Summary and conclusions. Br J Cancer 2000;83:561-5. |
| 29. | Nwankwo KC, Aniebue UU, Aquwa EN, Anarado AN, Agunwah E. Knowledge attitudes and practices of cervical cancer screening among urban and rural Nigerian women: A call for education and mass screening. Eur J Cancer Care (Engl) 2011;20:362-7. |
| 30. | Tefera F, Mitiku I. Uptake of cervical cancer screening and associated factors among 15 – 49-year-old women in Dessie Town, Northeast Ethiopia. J Cancer Educ 2016;32. doi: 10.1007/s13187-016-1021-6. |
| 31. | Chiqbu CO, Aniebue U. Why Southeastern Nigerian women who are aware of cervical cancer screening do not go for cervical cancer screening. Int J Gynecol Cancer 2011;21:1282-6. |
| 32. | Omenge E, Wachira J, Asirwa FC, Busakhale N, Naanyu V, Kisuya J, et al. Factors associated with uptake of Visual Inspection with Acetic Acid (VIA) for cervical cancer screening in Western Kenya. PLoS One 2016;11:1-12. |
| 33. | Islam RM, Bell RJ, Billah B, Hossain MB, Davis SR. Lack of understanding of cervical cancer and screening is the leading barrier to screening uptake in women at midlife in Bangladesh: Population-based cross-sectional survey. Oncologist 2015;20:1386-92. |
| 34. | Jain N, Halder A, Mehrotra R. A mixed method research to identify perceived reasons and solutions for low uptake of cervical cancer screening in urban families of Bhopal region. Scientifica 2016. doi: 10.1155/2016/5731627. |
| 35. | Roy B, Tang TS. Cervical cancer screening in Kolkata, India: Beliefs and predictors of cervical cancer screening among women attending a women's health clinic in Kolkata, India. 2008;23:253-9. |
| 36. | Were E, Nyaberi Z, Buziba N. Perceptions of risk and barriers to cervical cancer screening at Moi Teaching and Referral Hospital (MTRH), Eldoret, Kenya. Afr Health Sci 2011;11:58-64 |
| 37. | Kahesa C, Kjaer S, Mwaiselage J, Ngoma T, Tersbol B, Dartell M. Determinants of acceptance of cervical cancer screening in Dar esSalaam, Tanzania. BMC Public Health 2012;12:1093. |
| 38. | Ncube B, Bey A, Knight J, Bessler P, Jolly PE. Factors associated with the uptake of cervical cancer screening among women in Portland, Jamaica. N Am J Med Sci 2015;7:104-13. |
| 39. | Rossera JI, Njoroge B, Huchko MJ. Knowledge about cervical cancer screening and perception of risk among women attending outpatient clinics in rural Kenya. Int J Gynaecol Obstet 2015;128:211-5. |
| 40. | Cunningham MS, Skrastins E, Fitzpatrick R, Jindal P, Oneka O, Yeates K, et al. Cervical cancer screening and HPV vaccine acceptability among rural and urban women in Kilimanjaro Region, Tanzania. BMJ Open 2015;5:e005828. |
| 41. | Reis N, Bebis H, Kose S, Sis A, Engin R, Yavan T. Knowledge, behavior and beliefs related to cervical cancer and screening among Turkish women. Asian Pac J Cancer Prev 2012;13:1463-70. |
| 42. | Conde-Ferraez L, Suarez Allen RE, Carrillo Martinez JR, Ayora-Talavera G, Gonzalez-Losa Mdel R. Factors Associated with Cervical Cancer Screening Amongst Women of Reproductive Age from Yucatan, Mexico. Asian Pac J Cancer Prev 2012;13:4719-24. |
| 43. | Basu P, Sarkar S, Mukherjee S. Women ' s perceptions and social barriers determine compliance to cervical screening: Results from a population based study in India. Cancer Detect Prev 2006; 30:369-74. |
| 44. | Marva ML. Knowledge about cervical cancer prevention and psychosocial barriers. J Psychosom Obstet Gynaecol 2013;8942:163-9. |
| 45. | Watkins MM, Gabali C, Winkleby M, Gaona E, Lebaron S. Barriers to cervical cancer screening in rural Mexico. Int J Gynecol Cancer 2002;12:475-9. |
| 46. | Budkaew J, Chumworathayi B. Factors associated with decisions to attend cervical cancer screening among women aged 30-60 years in Chatapadung contracting medical unit, Thailand. Asian Pac J Cancer Prev 2014;15:4903-7. |
| 47. | Jia Y, Li S, Yang R, Zhou H, Xiang Q, Hu T, et al. Knowledge about cervical cancer and barriers of screening program among women in Wufeng County, a high-incidence region of cervical cancer in China. PLoS One 2013;8:2-8. |
| 48. | Sudenga SL, Rositch AF, Otieno WA, Smith JS. Brief report: Knowledge, attitudes, practices and perceived risk of cervical cancer among Kenyan women. Int J Gynecol Cancer 2013;23:895-9. |
| 49. | Bayu H, Berhe Y, Mulat A, Alemu A. Cervical cancer screening service uptake and associated factors among age eligible women in Mekelle zone, Northern Ethiopia, 2015: A community based study using health belief model. PLoS One 2016;11:1-13. |
| 50. | Rosser JI, Njoroge B, Huchko MJ. Changing knowledge, attitudes, and behaviors regarding cervical cancer screening: The effects of an educational intervention in rural Kenya. Patient Educ Couns 2015;98:884-9. |
| 51. | Abiodun OA, Olu-Abiodun OO, Sotunsa JO, Oluwole FA. Impact of health education intervention on knowledge and perception of cervical cancer and cervical screening uptake among adult women in rural communities in Nigeria. BMC Public Health 2014;14:814. |
| 52. | Wright KO, Faseru B, Kuyinu YA, Faduyile FA. Awareness and uptake of the Pap smear among market women in Lagos, Nigeria. J Public Health Africa 2011;2:58-62. |
| 53. | Modibbo F, Iregbu KC, Okuma J, Leeman A, Kasius A, de Koning M, et al. Randomized trial evaluating self-sampling for HPV DNA based tests for cervical cancer screening in Nigeria. Infect Agent Cancer 2017;12:11. |
| 54. | Mbachu C, Dim C, Ezeoke U. Effects of peer health education on perception and practice of screening for cervical cancer among urban residential women in south-east Nigeria: A before and after study. BMC Womens Health 2017;17:41. |
| 55. | Chigbu CO, Onyebuchi AK, Egbuji CC, Ezugwu EC. Experiences and unmet needs of women undergoing Pap smear cervical cancer screening: Impact on uptake of cervical cancer screening in South Eastern Nigeria. J Cancer Educ 2015;30:81-5. |
| 56. | Kocaöz S, Özçelik H, Talas MS, Akkaya F, Özkul F, Kurtuluş A, et al. The effect of education on the early diagnosis of breast and cervix cancer on the women's attitudes and behaviors regarding participating in screening programs. J Cancer Educ 2018;33:821-32. |
| 57. | Guvenc G, Akyuz A, Yenen MC. Effectiveness of nursing interventions to increase pap smear test screening. Res Nurs Health 2013;36:146-57. |
| 58. | Demirtas B, Acikgoz I. Promoting attendance at cervical cancer screening: Understanding the relationship with Turkish womens' health beliefs. Asian Pac J Cancer Prev 2013;14:333-40. |
| 59. | Alfaro KM, Gage JC, Rosenbaum AJ, Ditzian LR, Maza M, Scarinci IC, et al. Factors affecting attendance to cervical cancer screening among women in the Paracentral Region of El Salvador: A nested study within the CAPE HPV screening program. BMC Public Health 2015;15:1058. |
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2], [Table 3]
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